Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-26T12:44:17.601Z Has data issue: false hasContentIssue false
  • English
  • Français

Competition between honeydew producers in an ant–hemipteran interaction may enhance biological control of an invasive pest

Published online by Cambridge University Press:  14 August 2013

A. Tena ,
C.D. Hoddle  and
M.S. Hoddle
A. Tena*
Affiliation:
Unidad Asociada de Entomología UJI-IVIA-CIB CSIC, Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones Agrarias, IVIA, Spain
C.D. Hoddle
Affiliation:
Department of Entomology, University of California, 900 University Avenue, Riverside, CA 92521, USA
M.S. Hoddle
Affiliation:
Department of Entomology, University of California, 900 University Avenue, Riverside, CA 92521, USA Center for Invasive Species Research, University of California, Riverside, CA 92521, USA
*
*Author for correspondence Phone: (+34) 96 342 41 51 Fax: (+34) 96 342 40 01 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is an invasive citrus pest in southern California, which secretes honeydew and has the potential to spread a lethal bacterial disease, huanglongbing, of citrus. In urban citrus, Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae), also an invasive pest, tends honeydew-producing hemipterans. We used field data to determine whether the mutualistic relationship between L. humile and six established species of honeydew producers may hinder or favor the establishment of D. citri and its biological control with Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) in citrus via competition or mutualism for ants, respectively. In the field, L. humile and D. citri are engaged in a mutualistic relationship. Ants harvest solid honeydew secreted by psyllid nymphs and tended more than 55% of observed D. citri colonies. Linepithema humile displayed a preference hierarchy when tending honeydew producers infesting citrus. It responded equally or less intensively to D. citri than to other honeydew-producing species. Consequently, the mutualism between L. humile and D. citri was affected by the presence of other honeydew-producing species, and the percentage of D. citri colonies tended by L. humile. The number of ants per D. citri colony also decreased as the number of other honeydew producers increased. Diaphorina citri density was also affected by the presence of other honeydew producers. Both colony size and the number of D. citri nymphs counted per tree decreased as the number of other honeydew producers increased. Our results indicate that competition between honeydew producers for the mutualist ant L. humile may hinder the establishment of D. citri by possibly facilitating increased biological control.

Keywords

Diaphorina citriLinepithema humileTamarixia radiataant-attendancemutualism
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 6 , December 2013 , pp. 714 - 723
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Addicott, J.H. (1978) Competition for mutualists: aphids and ants. Canadian Journal of Zoology 56, 2093–2096.Google Scholar
Addicott, J.H. (1979) A multispecies aphid-ant association: density dependence and species-specific effects. Canadian Journal of Zoology 57, 558–569.Google Scholar
Banks, C.J. (1962) Effects of the ant, Lasius niger, on insects preying on small populations of Aphis fabae on bean plants. Annals of Applied Biology 50, 669–679.CrossRefGoogle Scholar
Billick, I. & Tonkel, K. (2003) The relative importance of spatial vs temporal variability in generating a conditional mutualism. Ecology 84, 289–295.Google Scholar
Breslow, N.E. & Clayton, D.G. (1993) Approximate inference in generalized linear mixed models. Journal of the American Statistical Association 88, 9–25.Google Scholar
Breton, L.M. & Addicott, J.F. (1992) Density-dependent mutualism in an aphid-ant interaction. Ecology 73, 2175–2180.CrossRefGoogle Scholar
Bristow, C.M. (1984) Differential benefits from ant attendance to two species of Homoptera on New York ironweed. Journal of Animal Ecology 53, 715–726.Google Scholar
Bristow, C.M. (1991) Why are so few aphids ant-tended? pp. 104–199in Huxley, C.R. & Cutler, D.F. (Eds) Ant-plant Interactions. Oxford, Oxford University Press.Google Scholar
Bonabeau, E., Theraulaz, G., Deneubourg, J.L., Aron, S. & Camazine, S. (1997) Self-organization in social insects. Trends in Ecology and Evolution 12, 188–193.Google Scholar
Bonser, R., Wright, P.J., Bament, S. & Chukwu, U.O. (1998) Optimal patch use by foraging workers of Lasius fuliginosus, L. niger and Myrmica ruginodis. Ecological Entomology 23, 15–31.Google Scholar
Bové, J. (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88, 7–37.Google Scholar
Buckley, R.C. & Gullan, P.J. (1991) More aggressive ant species (Hymenoptera: Formicidae) provide better protection for soft scales and mealybugs (Homoptera: Coccidae, Pseudococcidae). Biotropica 23, 282–286.Google Scholar
Chien, C.C., Chiu, S.C. & Ku, S.C. (1989) Biological control of Diaphorina citri in Taiwan. Fruits 44, 401–407.Google Scholar
Cushman, J.H. (1991) Host plant mediation of insect mutualism; variable outcomes in herbivore-ant interactions. Oikos 61, 138–144.Google Scholar
Cushman, J.H. & Addicott, J.F. (1991) Conditional interactions in ant-herbivore mutualisms. pp. 92–103in Huxley, C.R. & Cutler, D.F. (Eds) Ant-plant Interactions. Oxford, Oxford University Press.CrossRefGoogle Scholar
Cushman, J.H. & Whitham, T.G. (1989) Conditional mutualism in a membracid-ant association: temporal, age-specific, and density-dependent effects. Ecology 70, 1040–1047.Google Scholar
Cushman, J.H. & Whitham, T.G. (1991) Competition mediating the outcome of a mutualism: protective services of ants as a limiting resource for membracids. American Naturalist 138, 851–865.Google Scholar
Davidson, D.W. (1978) Experimental tests of the optimal diet in two social insects. Behavioural Ecology and Sociobiology 4, 35–51.Google Scholar
DeBach, P., Fleschner, C.A. & Dietrick, E.J. (1951) A biological check method for evaluating effectiveness of entomophagous insects. Journal of Economic Entomology 44, 763–766.Google Scholar
Fischer, M.K., Völkl, W. & Hoffmann, K.H. (2001) Competition for mutualists in an ant-homopteran interaction mediated by hierarchies of ant-attendance. Oikos 92, 531–541.Google Scholar
Flatt, T. & Weisser, W.W. (2000) The effects of mutualistic ants on aphid life history traits. Ecology 81, 3522–3529.Google Scholar
French, J.V., Kahlke, C.J. & da Gracía, J.V. (2001) First record of the Asian citrus psylla, Diaphorina citri Kuwayama (Homoptera: Psyllidae) in Texas. Subtropical Plant Science 53, 14–15.Google Scholar
Grafton-Cardwell, E.E., Stelinski, L.L. & Stansly, P.A. (2013) Biology and management of Asian citrus psyllid, vector of the huanglongbing pathogens. Annual Reviews of Entomology 58, 413–432.CrossRefGoogle ScholarPubMed
Halbert, S.E. & Manjunath, K.L. (2004) Asian citrus psyllid (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Florida Entomologist 87, 330–353.CrossRefGoogle Scholar
Harmon, P.J. & Andow, D.A. (2007) Behavioral mechanisms underlying ants’ density-dependent deterrence of aphid-eating predators. Oikos 116, 1030–1036.Google Scholar
Hoddle, M.S. (2013) Urban warfare: Pakistani parasitoids tackle Asian citrus psyllid in backyard citrus. Citrograph (in press).Google Scholar
Itioka, T. & Inoue, T. (1996) Density-dependent ant attendance and its effects on the parasitism of a honeydew-producing scale insect, Ceroplastes rubens. Oecologia 106, 448–454.Google Scholar
James, D.G., Stevens, M.M. & O'Malley, K.J. (1997) The impact of foraging ants on populations of Coccus hesperidum L. (Hem., Coccidae) and Aonidiella aurantii (Maskell) (Hem., Diaspididae) in an Australian citrus grove. Journal of Applied Entomology 121, 257–259.CrossRefGoogle Scholar
Kaneko, S. (2003) Different impacts of two species of aphid tending ants with different aggressiveness on the number of emerging adults of the aphid's primary parasitoid and hyperparasitoids. Ecological Research 18, 199–212.Google Scholar
Klotz, J.H., Rust, M.K. & Phillips, P. (2004) Liquid bait delivery systems for controlling Argentine ants in citrus groves (Hymenoptera: Formicidae). Sociobiology 43, 419–427.Google Scholar
Liebhold, A.M. & Tobin, P.C. (2008) Population ecology of insect invasions and their management. Annual Review of Entomology 53, 387–408.CrossRefGoogle ScholarPubMed
Mailleux, A.C., Detrain, C. & Deneubourg, J. (2000) How do the ants assess food volume? Animal Behaviour 59, 1061–1069.CrossRefGoogle ScholarPubMed
Mailleux, A.C., Deneubourg, J.L. & Detrain, C. (2003) Regulation of ants’ foraging to resource productivity. Proceedings of the Royal Society of London Series B, Biological Sciences 270, 1609–1616.Google Scholar
McCullagh, P. & Nelder, J. (1989) Generalized Linear Models. London, Chapman and Hall.Google Scholar
Michaud, J.P. (2004) Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biological Control 29, 260–269.Google Scholar
Morales, M.A. (2000) Mechanisms and density dependence of benefit in an ant–membracid mutualism. Ecology 81, 482–489.Google Scholar
Moreno, D.S., Haney, P.B. & Luck, R.F. (1987) Chlorpyrifos and diazinon as barriers to Argentine ant (Hymenoptera: Formicidae) foraging on citrus trees. Journal of Economic Entomology 80, 208–214.Google Scholar
Müller, C.B. & Godfray, H.C.J. (1999) Indirect interactions in aphid–parasitoid communities. Researches on Population Ecology 41, 93–106.Google Scholar
Noe, R. & Hammerstein, P. (1994) Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral ecology and sociobiology 35, 1–11.Google Scholar
Nonacs, P. & Dill, L.M. (1991) Mortality risk vs food quality trade-offs in a common currency: ant path preferences. Ecology 71, 1886–1892.Google Scholar
Pekas, A., Tena, A., Aguilar, A. & Garcia-Marí, F. (2010) Effect of Mediterranean ants (Hymenoptera: Formicidae) on California red scale Aonidiella aurantii (Hemiptera: Diaspididae) populations in citrus orchards. Environmental Entomology 39, 827–834.CrossRefGoogle ScholarPubMed
Pekas, A., Tena, A., Aguilar, A. & Garcia-Marí, F. (2011) Spatio-temporal patterns and interactions with honeydew-producing hemiptera of ants in a Mediterranean citrus orchard. Agricultural and Forest Entomology 13, 89–97.Google Scholar
Qureshi, J.A. & Stansly, P.A. (2009) Exclusion techniques reveal significant biotic mortality suffered by Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae) populations in Florida citrus. Biological Control 50, 129–136.CrossRefGoogle Scholar
Qureshi, J.A., Rogers, M.E., Hall, D.G. & Stansly, P.A. (2009) Incidence of invasive Diaphorina citri (Hemiptera: Psyllidae) and its introduced parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) in Florida citrus. Journal of Economic Entomology 102, 247–256.Google Scholar
Shik, J.Z. & Silverman, J. (2013) Towards a nutritional ecology of invasive establishment: aphid mutualists provide better fuel for incipient Argentine ant colonies than insect prey. Biological Invasions. Doi: 10.1007/s10530-012-0330-x 2013 15, 829–836.Google Scholar
Styrsky, J.D. & Eubanks, M.D. (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proceedings of the Royal Society B: Biological Sciences 274, 151–164.Google Scholar
Tena, A., Pekas, A., Wäckers, F. & Urbaneja, A. (2013) Energy reserves of parasitoids depend on honeydew from non-hosts. Ecological Entomology 38(3), 278–289, June 2013.Google Scholar
Teresa Martinez-Ferrer, M., Grafton-Cardwell, E.E. & Shorey, H.H. (2003) Disruption of parasitism of the California red scale (Homoptera: Diaspididae) by three ant species (Hymenoptera: Formicidae). Biological Control 26, 279–286.Google Scholar
van Veen, F.F.J., Morris, R.J. & Godfray, H.C.J. (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annual Review of Entomology 51, 187–208.Google Scholar
Vega, S.J. & Rust, M.K. (2001) The Argentine ant – a significant invasive species in agricultural, urban and natural environments. Sociobiology 37, 3–25.Google Scholar
Völkl, W. (1992) Aphids or their parasitoids: who actually benefits from ant-attendance? Journal of Animal Ecology 61, 273–281.CrossRefGoogle Scholar
Völkl, W., Woodring, J., Fischer, M., Lorenz, M.W. & Hoffmann, K.H. (1999) Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia 118, 483–491.Google ScholarPubMed
Way, M.J. (1963) Mutualism between ants and honeydew-producing Homoptera. Annual Review of Entomology 8, 307–344.Google Scholar
Woodring, J., Wiedemann, R., Fischer, M.K., Hoffmann, K.H. & Völkl, W. (2004) Honeydew amino acids in relation to sugars and their role in the establishment of ant – attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare). Physiological Entomology 29, 311–319.Google Scholar